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Effect of supplementary zinc on orthodontic tooth movement in a rat model

ABSTRACT

Introduction:

Osteoclasts and osteoblasts are responsible for regulating bone homeostasis during which the trace element zinc has been shown to exert a cumulative effect on bone mass by stimulating osteoblastic bone formation and inhibiting osteoclastic bone resorption.

Objective:

The aim of the present study was to investigate the effects of zinc (Zn) on orthodontic tooth movement (OTM) in a rat model.

Material and Methods:

A total of 44 male Wistar rats were divided into four groups of 11 animals each and received 0, 1.5, 20 and 50 ppm Zn in distilled water for 60 days. In the last 21 days of the study, nickel-titanium closed coil springs were ligated between maxillary right incisors and first molars of all rats, and tooth movement was measured at the end of this period. Histological analysis of hematoxylin/eosin slides was performed to assess root resorption lacunae, osteoclast number and periodontal ligament (PDL) width.

Results:

Mean OTM was calculated as 51.8, 49.1, 35.5 and 45 µm in the 0, 1.5, 20 and 50 ppm zinc-receiving groups, respectively. There were no significant differences in neither OTM nor histological parameters among the study groups (p > 0.05).

Conclusion:

According to the results obtained in the current investigation, increase in supplementary zinc up to 50 ppm does not affect the rate of OTM neither bone and root resorption in rats.

Keywords:
Dietary supplement; Orthodontics; Tooth movement; Zinc

RESUMO

Introdução:

os osteoclastos e os osteoblastos são responsáveis por regular a homeostase óssea, processo no qual o oligoelemento zinco tem demonstrado exercer um efeito cumulativo sobre a massa óssea, estimulando a formação óssea osteoblástica e inibindo a reabsorção óssea osteoclástica.

Objetivo:

o objetivo do presente estudo foi investigar os efeitos do zinco (Zn) sobre a movimentação dentária ortodôntica (MDO) em ratos.

Métodos:

um total de 44 ratos Wistar machos foi dividido em quatro grupos de 11 animais cada, os quais receberam 0; 1,5; 20 e 50ppm de zinco diluído em água destilada, durante 60 dias. Nos últimos 21 dias do estudo, molas helicoidais fechadas de níquel-titânio foram instaladas entre os incisivos direitos e os primeiros molares superiores de todos os ratos, e a movimentação dentária foi medida ao final desse período. Foi realizada análise histológica de cortes corados por hematoxilina-eosina, para avaliar as lacunas de reabsorção radicular, o número de osteoclastos e a espessura do ligamento periodontal.

Resultados:

as médias da MDO foram estimadas em 51,8; 49,1; 35,5 e 45µm no grupos que receberam, respectivamente, 0; 1,5; 20 e 50ppm de zinco. Não houve diferença significativa entre os grupos experimentais, nem quanto à MDO, nem quanto aos parâmetros histológicos (p > 0,05).

Conclusão:

segundo os resultados obtidos na presente investigação, verificou-se que um aumento na dose de suplementação com zinco para 50ppm não afeta nem o índice de MDO, nem a reabsorção óssea ou radicular em ratos.

Palavras-chave:
Suplementação alimentar; Ortodontia; Movimentação dentária; Zinco

INTRODUCTION

Zinc (Zn) is an essential trace element that serves as a cofactor for more than 200 enzymes, and being a constituent of nearly all human cell types, plays a major role in a number of basic biological processes including proliferation, wound healing, immunity and osteogenesis.11. Czerwinski AW, Clark ML, Serafetinides EA, Perrier C, Huber W. Safety and efficacy of zinc sulfate in geriatric patients. Clin Pharmacol Ther. 1974 Apr;15(4):436-41. Deficiency of this fundamental mineral is a universal health issue, especially during adolescence due to the occurrence of growth spurts. This has led to the recognition of a need for improved public health programs to support individuals with Zn deficiency known to comprise half the world's population.22. Kawade R. Zinc status and its association with the health of adolescents: a review of studies in India. Glob Health Action. 2012;5:7353. Delayed bone maturation and impaired growth are two of the major consequences of insufficient Zn intake in pubescent individuals who are being treated worldwide by prescription of Zn supplements as part of their treatment regimen.33. Dekker LH, Villamor E. Zinc supplementation in children is not associated with decreases in hemoglobin concentrations. J Nutr. 2010 May;140(5):1035-40. In addition to the bone-related applications of this substance, different compounds, such as zinc gluconate glycine and zinc acetate, are routinely used as anti-cold agents.44. Taylor DM, Liyanage JA, Williams DR, Harding KG. A new approach to monitoring trace element concentrations and speciation in wounds and wound fluids. Appl Radiat Isot. 1998 May-Jun;49(5-6):677-9.

Zn impacts bone metabolism via augmentation of osteoblastic activity and down regulation of osteoclastic bone resorption, a fact reported by numerous investigations.55. Yamaguchi M. Nutritional factors and bone homeostasis: synergistic effect with zinc and genistein in osteogenesis. Mol Cell Biochem. 2012 July;366(1-2):201-21.

6. Igarashi A, Yamaguchi M. Increase in bone protein components with healing rat fractures: enhancement by zinc treatment. Int J Mol Med. 1999 Dec;4(6):615-20.

7. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303.
-88. Abrisham SM, Yaghmaei M, Abbas FM, Sharifi D, Abrisham SM. Effect of oral zinc therapy on osteogenesis in rabbits. J Oral Maxillofac Surg. 2010 July;68(7):1676-80. Bone remodeling is the foundation of orthodontic treatment and tooth movement relies on this phenomenon.99. Meikle MC. The tissue, cellular, and molecular regulation of orthodontic tooth movement: 100 years after Carl Sandstedt. Eur J Orthod. 2006 Jun;28(3):221-40. Following the application of orthodontic forces, the periodontium responds by an inflammatory reaction leading to reorganization of its cellular components and a modification in its equilibrium in favor of bone remodeling, the end result of which would be tooth movement.1010. Pizzo G, Licata ME, Guiglia R, Giuliana G. Root resorption and orthodontic treatment. Review of the literature. Minerva Stomatol. 2007 Jan-Feb;56(1-2):31-44.,1111. Brezniak N, Wasserstein A. Orthodontically induced inflammatory root resorption. Part I: The basic science aspects. Angle Orthod. 2002 Apr;72(2):175-9.,1212. Storey E. The nature of tooth movement. Am J Orthod. 1973 Mar;63(3):292-314.

Several authors have studied the effects of local and systemic medicaments, including dietary supplements on orthodontic tooth movement (OTM).1313. Gameiro GH, Pereira-Neto JS, Magnani MB, Nouer DF. The influence of drugs and systemic factors on orthodontic tooth movement. J Clin Orthod. 2007 Feb;41(2):73-8; quiz 71.

14. Tyrovola JB, Spyropoulos MN. Effects of drugs and systemic factors on orthodontic treatment. Quintessence Int. 2001 May;32(5):365-71.

15. Krishnan V, Davidovitch Z. The effect of drugs on orthodontic tooth movement. Orthod Craniofac Res. 2006;9(4):163-71.
-1616. Bartzela T, Türp JC, Motschall E, Maltha JC. Medication effects on the rate of orthodontic tooth movement: a systematic literature review. Am J Orthod Dentofacial Orthop. 2009 Jan;135(1):16-26. A considerable number of patients seeking orthodontic treatment may be using medications due to general health problems; moreover, regarding the prevailing trend towards the increased use of dietary supplements among these individuals, having some notion of the effect of various drugs on OTM would be helpful for treatment planning and predicting the length of these treatment modalities.1717. Isaacson JR. Your patients are on drugs [editorial]. Angle Orthod. 2000;70(2):96. Considering the osteogenic potential of Zn, along with its inhibiting impact on bone resorption,77. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303. it was hypothesized that this substance might negatively regulate the rate of OTM in rats. Since Zn supplementation is becoming prevalent among patients, the present study was designed to investigate the effect of this micronutrient on tooth movement in rats.

MATERIAL AND METHODS

Animals

The experimental protocol of the current study was approved by the Ethics Committee of Tehran University of Medical Sciences (code: 91-01-70-17586-55909). A total of 44 male Wistar rats (200-250 g) were housed in plastic cages, maintained on a 12/12 hour light-dark cycle and randomly divided into four groups (n = 11) with free access to standard laboratory chow. Their drinking water consisted of double distilled water with Zn sulfate added at concentrations of 0, 1.5, 20 and 50 ppm for use in the control group and groups 1, 2 and 3, respectively.1818. Brzóska MM, Galazyn-Sidorczuk M, Rogalska J, Roszczenko A, Jurczuk M, Majewska K, et al. Beneficial effect of zinc supplementation on biomechanical properties of femoral distal end and femoral diaphysis of male rats chronically exposed to cadmium. Chem Biol Interact. 2008 Feb 15;171(3):312-24.,1919. Brzóska MM, Rogalska J, Galazyn-Sidorczuk M, Jurczuk M, Roszczenko A, Kulikowska-Karpinska E, et al. Effect of zinc supplementation on bone metabolism in male rats chronically exposed to cadmium. Toxicology. 2007 July 31;237(1-3):89-103.,2020. Fong LY, Jiang Y, Rawahneh ML, Smalley KJ, Croce CM, Farber JL, et al. Zinc supplementation suppresses 4-nitroquinoline 1-oxide-induced rat oral carcinogenesis. Carcinogenesis. 2011 Apr;32(4):554-60. All animals were weighed at the beginning of the study (day 1), on the first day of appliance placement (day 40) and immediately before sacrifice (day 60).

Orthodontic treatment and measurement of tooth movement

On day 40th of the study period, each rat was anaesthetized with an intraperitoneal injection of xylazine HCL (6 mg/kg body weight) and ketamine (50 mg/kg body weight) in order to receive orthodontic appliances. Based on the method suggested by Nilforoushan et al,2222. Nilforoushan D, Shirazi M, Dehpour AR. The role of opioid systems on orthodontic tooth movement in cholestatic rats. Angle Orthod. 2002 Oct;72(5):476-80. nickel-titanium (NiTi) closed coil springs (NiTi, 3M Unitek, Monrovia, CA, Hitek, 0.006 × 0.022-in) were ligated between left maxillary first molars and incisors of all rats with 0.010-in stainless steel ligature wires to deliver a force of 60 g without further activation throughout the duration of the investigation. Labial and distal grooves cut, in approximation to the gingival margins of incisors, were used to retain the wires. The mesiolingual undercut of the first molar provided necessary retention in the posterior segment of the appliance. Two incisors were attached together by means of composite resin (Transbond XT, 3M Unitek, Monrovia, Calif) to achieve anterior anchorage and ensure mesial movement of molars.2121. Shirazi M, Khosrowshahi M, Dehpour AR. The effect of chronic renal insufficiency on orthodontic tooth movement in rats. Angle Orthod. 2001 Dec;71(6):494-8. Moreover, composite resin covered the anterior ligatures to preserve the wires during the study period. This was followed by 1.5 mm reduction of mandibular incisors with a high-speed handpiece in order to prevent severance of the ligature wires.2222. Nilforoushan D, Shirazi M, Dehpour AR. The role of opioid systems on orthodontic tooth movement in cholestatic rats. Angle Orthod. 2002 Oct;72(5):476-80.,2323. Sirisoontorn I, Hotokezaka H, Hashimoto M, Gonzales C, Luppanapornlarp S, Darendeliler MA, et al. Orthodontic tooth movement and root resorption in ovariectomized rats treated by systemic administration of zoledronic acid. Am J Orthod Dentofacial Orthop. 2012 May;141(5):563-73. At the beginning of the study, none of the animals demonstrated any kind of space between first and second molars and all contacts were intact.

After orthodontic treatment, the standard rat chow was ground to provide a soft diet for the purpose of minimizing any discomfort and diminishing the chance of dislodgement or damage to the appliances.

All animals were sacrificed on day 60th of the study period by ether overdose followed by decapitation. A feeler gauge was employed to assess mesial movement of first molar by measuring the space between first and second molars before removal of the appliances, so as to prevent any possible distal relapse of the first molar. All measurements were repeated twice by the same operator blinded to the study groups, and the means were used for statistical analysis.

Histological evaluation

The maxillae were separated, fixed in 10% formalin for five days and immersed in 5% formic acid until adequately decalcified (an average of five days). Sequential 5-µm serial sections were prepared from each paraffin block and the five sections containing the largest root area were chosen and analyzed histomorphometrically, as described previously.2424. Hakami Z, Kitaura H, Kimura K, Ishida M, Sugisawa H, Ida H, et al. Effect of interleukin-4 on orthodontic tooth movement and associated root resorption. Eur J Orthod. 2015 Feb;37(1):87-94.,2525. Taddei SR, Andrade I Jr, Queiroz-Junior CM, Garlet TP, Garlet GP, Cunha FQ, et al. Role of CCR2 in orthodontic tooth movement. Am J Orthod Dentofacial Orthop. 2012 Feb;141(2):153-60. The final value was expressed as the mean of the selected sections.2626. Leiker BJ, Nanda RS, Currier GF, Howes RI, Sinha PK. The effects of exogenous prostaglandins on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop. 1995 Oct;108(4):380-8. The mesial root was histomorphometrically evaluated on the section containing the full length of the root from the cemento-enamel junction (CEJ) to the apex, by means of a double-headed Olympus BX-41 light microscope equipped with a digital camera (DP25 Olympus) and analysis software (DP2-BSW, Olympus). The number of osteoclasts, periodontal ligament (PDL) width, number of resorption lacunae and their depths and widths were analyzed by two observers, and disagreements were solved by consensus.2727. Sekhavat AR, Mousavizadeh K, Pakshir HR, Aslani FS. Effect of misoprostol, a prostaglandin E1 analog, on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop. 2002 Nov;122(5):542-7. The width of the PDL was determined coronally and apically on both mesial and distal aspects of the mesial root.2727. Sekhavat AR, Mousavizadeh K, Pakshir HR, Aslani FS. Effect of misoprostol, a prostaglandin E1 analog, on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop. 2002 Nov;122(5):542-7.,2828. Tengku BS, Joseph BK, Harbrow D, Taverne AA, Symons AL. Effect of a static magnetic field on orthodontic tooth movement in the rat. Eur J Orthod. 2000 Oct;22(5):475-87. All sections were measured twice by both observers on the double-headed microscope, and the mean of the two values was used in all consecutive calculations.

Statistical analysis

Differences among groups were analyzed by one-way ANOVA followed by Tukey post-hoc tests for multiple comparisons. Probability values p < 0.05 were considered statistically significant.

RESULTS

There was a gradual increase in rats' weight during our investigation, and none of them died or demonstrated weight loss throughout the study period. No significant differences in mean overall weights were found among the four study groups (p = 0.25). All treated first molars shifted mesially into the space between molars and incisors (Table 1). The highest and lowest amounts of tooth movement were observed in the control and 20 ppm Zn groups, respectively; but there were no significant differences among groups (p = 0.18).

Table 1
Molar separation over 21 days.

Descriptive histological data are shown in Table 2. Osteoclast numbers and resorptive lacunae widths and depths showed no significant differences among study groups (Table 2). Of the four measured locations of PDL width, significant difference was found only in the disto-apical area (Table 2) among groups. Based on multiple comparisons, PDL width was significantly higher in group 1 (1.5 ppm) compared to the control group (p = 0.02).

Table 2
Descriptive histological data.

DISCUSSION

Zn supplements are prescribed for adults for numerous reasons. Among the various nutritional attributes of Zn, inhibition of bone resorption and stimulation of bone growth and mineralization77. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303. might directly influence OTM induced by orthodontic treatment. Several studies have investigated the effects of Zn on various aspects of bone quality,55. Yamaguchi M. Nutritional factors and bone homeostasis: synergistic effect with zinc and genistein in osteogenesis. Mol Cell Biochem. 2012 July;366(1-2):201-21.,2929. Kara C, Orbak R, Dagsuyu IM, Orbak Z, Bilici N, Gumustekin K. In vivo assessment of zinc deficiency on craniofacial growth in a rat model. Eur J Dent. 2009 Jan;3(1):10-5. and its deficiency has been suggested to play a role in the development of osteoporosis.3030. Eberle J, Schmidmayer S, Erben RG, Stangassinger M, Roth HP. Skeletal effects of zinc deficiency in growing rats. J Trace Elem Med Biol. 1999;13(1-2):21-6.

In the present study, we measured the amount of tooth movement in rats receiving 0 to 50 ppm zinc sulfate, followed by application of a simple orthodontic appliance, and did not observe significant difference among groups, which was also confirmed by our histomorphometric analysis. The present result was in agreement with a study conducted by Abrisham et al88. Abrisham SM, Yaghmaei M, Abbas FM, Sharifi D, Abrisham SM. Effect of oral zinc therapy on osteogenesis in rabbits. J Oral Maxillofac Surg. 2010 July;68(7):1676-80. who also did not find Zn to be effective in bone healing and reported no significant relationship between this substance and bone formation in rabbits. Similarly, a periodontal study in rats failed to demonstrate differences in pocket depths between animals receiving Zn-containing diets and those deficient in this micronutrient.3131. Orbak R, Kara C, Ozbek E, Tezel A, Demir T. Effects of zinc deficiency on oral and periodontal diseases in rats. J Periodontal Res. 2007;42(2):138-43. In contrast to our findings, Zn has been shown to prevent osteoporosis3232. Yamaguchi M. Role of nutritional zinc in the prevention of osteoporosis. Mol Cell Biochem. 2010;338(1-2):241-54. and induce osteogenesis.55. Yamaguchi M. Nutritional factors and bone homeostasis: synergistic effect with zinc and genistein in osteogenesis. Mol Cell Biochem. 2012 July;366(1-2):201-21.

Previous investigations have indicated that the duration of Zn application may have an impact on its expected bone effects. Accordingly, any possible positive function of this micronutrient diminishes with time.88. Abrisham SM, Yaghmaei M, Abbas FM, Sharifi D, Abrisham SM. Effect of oral zinc therapy on osteogenesis in rabbits. J Oral Maxillofac Surg. 2010 July;68(7):1676-80.,3333. Yamaguchi M, Mochizuki A, Okada S. Stimulatory effect of zinc on bone growth in weanling rats. J Pharmacobiodyn. 1982;5(8):619-26. This may explain the lack of difference in OTM between control and Zn-receiving rats; consequently, the 40th day period of Zn administration prior to orthodontic treatment in the current investigation may have suppressed the activity of this element. For the same reason, it has been suggested that Zn should be prescribed at the initial stages of inflammatory reactions,3434. Kaplan B, Gönül B, Dinçer S, Dinçer Kaya FN, Babül A. Relationships between tensile strength, ascorbic acid, hydroxyproline, and zinc levels of rabbit full-thickness incision wound healing. Surg Today. 2004;34(9):747-51.,3535. Savlov ED, Strain WH, Huegin F. Radiozinc studies in experimental wound healing. J Surg Res. 1962 May;2:209-12. which is known to play a major role in tooth movement.3636. Alhashimi N, Frithiof L, Brudvik P, Bakhiet M. Orthodontic tooth movement and de novo synthesis of proinflammatory cytokines. Am J Orthod Dentofacial Orthop. 2001 Mar;119(3):307-12. Additionally, a number of studies have pointed out that Zn can only perform where its deficiency exists;3737. Hallböök T, Lanner E. Serum-zinc and healing of venous leg ulcers. Lancet. 1972 Oct 14;2(7781):780-2. thus, pretreatment supplementation administered in the present study might have reduced any chance of Zn inadequacy and, therefore, eliminated its possible impact on OTM.

Despite the insignificant difference among our study groups, a decrease in OTM occurred from the first dose of Zn up to 20 ppm, but increased in Group 3 in which rats received 50 ppm. The decrease could be justified based on the proposed anti-resorptive effects of Zn, but the reason for the increase may not be as simple to explain. Cerovic et al3838. Cerovic A, Miletic I, Sobajic S, Blagojevic D, Radusinovic M, El-Sohemy A. Effects of zinc on the mineralization of bone nodules from human osteoblast-like cells. Biol Trace Elem Res. 2007 Apr;116(1):61-71. also reported similar findings regarding alkaline phosphatase activity and in vitro bone nodule formation with increasing Zn concentrations, suggesting "biphasic effects" for this element in addition to other possible processes including cytotoxicity at higher doses.

Our histomorphometric findings showed no significant difference in osteoclast number among groups. This supports our clinical OTM data, but may seem contradictory to a number of former investigations demonstrating a down-regulating influence of Zn on osteoclastic resorptive potential and differentiation.77. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303.,3939. Yamaguchi M, Weitzmann MN. Zinc stimulates osteoblastogenesis and suppresses osteoclastogenesis by antagonizing NF-?B activation. Mol Cell Biochem. 2011 Sept;355(1-2):179-86.,4040. Park KH, Park B, Yoon DS, Kwon SH, Shin DM, Lee JW, et al. Zinc inhibits osteoclast differentiation by suppression of Ca2+-Calcineurin-NFATc1 signaling pathway. Cell Commun Signal. 2013 Oct 2;11:74. Nevertheless, osteoclastic number may not necessarily have a positive association with osteoclast function.4141. Karsdal MA, Martin TJ, Bollerslev J, Christiansen C, Henriksen K. Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res. 2007 Apr;22(4):487-94. Holloway et al4242. Holloway WR, Collier FM, Herbst RE, Hodge JM, Nicholson GC. Osteoblast-mediated effects of zinc on isolated rat osteoclasts: inhibition of bone resorption and enhancement of osteoclast number. Bone. 1996 Aug;19(2):137-42. reported inhibition of bone resorption following Zn treatment in osteoblastic/osteoclastic co-culture, but found increased osteoclastic numbers. However, the study situation (in vitro versus in vivo), detection methods and Zn administration in their research were different from those used in the present investigation.

The methods used in this study were selected based on previous research in this field;77. Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303.,4343. Watanabe T, Nakada H, Takahashi T, Fujita K, Tanimoto Y, Sakae T, et al. Potential for acceleration of bone formation after implant surgery by using a dietary supplement: an animal study. J Oral Rehabil. 2015 Jun;42(6):447-53. and, according to our findings, neither clinical nor histopathological changes were observed following Zn application in rats. Future studies using serum and/or urine analysis could help clarify the role of Zn in OTM and possibly confirm the conclusions of the current investigation. Additionally, further researches with immunohistochemical and molecular techniques are needed to understand the effect of Zn supplementation on bone remodeling during orthodontic treatment. If the present results are supported by future studies in animals and humans, the specific modifications in orthodontic treatment planning might not be necessary for patients receiving Zn as a dietary supplementation.

Regarding the four locations of PDL width measured in our study, significant difference was found only in the distoapical aspect among groups. The reason for this difference is not clear; further studies on various histopathologic features of OTM following Zn treatment are suggested to help clarify the role of this important micronutrient in orthodontic treatment.

CONCLUSIONS

According to the result obtained in the present study, systemic Zn supplementation up to 50 ppm does not affect OTM, neither bone nor root resorption in rats. Extrapolation of these findings to human subjects would require extensive research using more sophisticated techniques and drug concentrations.

Acknowledgments

This study has been funded and supported by Tehran University of Medical Sciences (TUMS); Grant # 132/872.

REFERENCES

  • 1
    Czerwinski AW, Clark ML, Serafetinides EA, Perrier C, Huber W. Safety and efficacy of zinc sulfate in geriatric patients. Clin Pharmacol Ther. 1974 Apr;15(4):436-41.
  • 2
    Kawade R. Zinc status and its association with the health of adolescents: a review of studies in India. Glob Health Action. 2012;5:7353.
  • 3
    Dekker LH, Villamor E. Zinc supplementation in children is not associated with decreases in hemoglobin concentrations. J Nutr. 2010 May;140(5):1035-40.
  • 4
    Taylor DM, Liyanage JA, Williams DR, Harding KG. A new approach to monitoring trace element concentrations and speciation in wounds and wound fluids. Appl Radiat Isot. 1998 May-Jun;49(5-6):677-9.
  • 5
    Yamaguchi M. Nutritional factors and bone homeostasis: synergistic effect with zinc and genistein in osteogenesis. Mol Cell Biochem. 2012 July;366(1-2):201-21.
  • 6
    Igarashi A, Yamaguchi M. Increase in bone protein components with healing rat fractures: enhancement by zinc treatment. Int J Mol Med. 1999 Dec;4(6):615-20.
  • 7
    Hadley KB, Newman SM, Hunt JR. Dietary zinc reduces osteoclast resorption activities and increases markers of osteoblast differentiation, matrix maturation, and mineralization in the long bones of growing rats. J Nutr Biochem. 2010 Apr;21(4):297-303.
  • 8
    Abrisham SM, Yaghmaei M, Abbas FM, Sharifi D, Abrisham SM. Effect of oral zinc therapy on osteogenesis in rabbits. J Oral Maxillofac Surg. 2010 July;68(7):1676-80.
  • 9
    Meikle MC. The tissue, cellular, and molecular regulation of orthodontic tooth movement: 100 years after Carl Sandstedt. Eur J Orthod. 2006 Jun;28(3):221-40.
  • 10
    Pizzo G, Licata ME, Guiglia R, Giuliana G. Root resorption and orthodontic treatment. Review of the literature. Minerva Stomatol. 2007 Jan-Feb;56(1-2):31-44.
  • 11
    Brezniak N, Wasserstein A. Orthodontically induced inflammatory root resorption. Part I: The basic science aspects. Angle Orthod. 2002 Apr;72(2):175-9.
  • 12
    Storey E. The nature of tooth movement. Am J Orthod. 1973 Mar;63(3):292-314.
  • 13
    Gameiro GH, Pereira-Neto JS, Magnani MB, Nouer DF. The influence of drugs and systemic factors on orthodontic tooth movement. J Clin Orthod. 2007 Feb;41(2):73-8; quiz 71.
  • 14
    Tyrovola JB, Spyropoulos MN. Effects of drugs and systemic factors on orthodontic treatment. Quintessence Int. 2001 May;32(5):365-71.
  • 15
    Krishnan V, Davidovitch Z. The effect of drugs on orthodontic tooth movement. Orthod Craniofac Res. 2006;9(4):163-71.
  • 16
    Bartzela T, Türp JC, Motschall E, Maltha JC. Medication effects on the rate of orthodontic tooth movement: a systematic literature review. Am J Orthod Dentofacial Orthop. 2009 Jan;135(1):16-26.
  • 17
    Isaacson JR. Your patients are on drugs [editorial]. Angle Orthod. 2000;70(2):96.
  • 18
    Brzóska MM, Galazyn-Sidorczuk M, Rogalska J, Roszczenko A, Jurczuk M, Majewska K, et al. Beneficial effect of zinc supplementation on biomechanical properties of femoral distal end and femoral diaphysis of male rats chronically exposed to cadmium. Chem Biol Interact. 2008 Feb 15;171(3):312-24.
  • 19
    Brzóska MM, Rogalska J, Galazyn-Sidorczuk M, Jurczuk M, Roszczenko A, Kulikowska-Karpinska E, et al. Effect of zinc supplementation on bone metabolism in male rats chronically exposed to cadmium. Toxicology. 2007 July 31;237(1-3):89-103.
  • 20
    Fong LY, Jiang Y, Rawahneh ML, Smalley KJ, Croce CM, Farber JL, et al. Zinc supplementation suppresses 4-nitroquinoline 1-oxide-induced rat oral carcinogenesis. Carcinogenesis. 2011 Apr;32(4):554-60.
  • 21
    Shirazi M, Khosrowshahi M, Dehpour AR. The effect of chronic renal insufficiency on orthodontic tooth movement in rats. Angle Orthod. 2001 Dec;71(6):494-8.
  • 22
    Nilforoushan D, Shirazi M, Dehpour AR. The role of opioid systems on orthodontic tooth movement in cholestatic rats. Angle Orthod. 2002 Oct;72(5):476-80.
  • 23
    Sirisoontorn I, Hotokezaka H, Hashimoto M, Gonzales C, Luppanapornlarp S, Darendeliler MA, et al. Orthodontic tooth movement and root resorption in ovariectomized rats treated by systemic administration of zoledronic acid. Am J Orthod Dentofacial Orthop. 2012 May;141(5):563-73.
  • 24
    Hakami Z, Kitaura H, Kimura K, Ishida M, Sugisawa H, Ida H, et al. Effect of interleukin-4 on orthodontic tooth movement and associated root resorption. Eur J Orthod. 2015 Feb;37(1):87-94.
  • 25
    Taddei SR, Andrade I Jr, Queiroz-Junior CM, Garlet TP, Garlet GP, Cunha FQ, et al. Role of CCR2 in orthodontic tooth movement. Am J Orthod Dentofacial Orthop. 2012 Feb;141(2):153-60.
  • 26
    Leiker BJ, Nanda RS, Currier GF, Howes RI, Sinha PK. The effects of exogenous prostaglandins on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop. 1995 Oct;108(4):380-8.
  • 27
    Sekhavat AR, Mousavizadeh K, Pakshir HR, Aslani FS. Effect of misoprostol, a prostaglandin E1 analog, on orthodontic tooth movement in rats. Am J Orthod Dentofacial Orthop. 2002 Nov;122(5):542-7.
  • 28
    Tengku BS, Joseph BK, Harbrow D, Taverne AA, Symons AL. Effect of a static magnetic field on orthodontic tooth movement in the rat. Eur J Orthod. 2000 Oct;22(5):475-87.
  • 29
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    The authors report no commercial, proprietary or financial interest in the products or companies described in this article.
  • Erratum

    In the article Effect of supplementary zinc on orthodontic tooth movement in a rat model, published at Dental Press J Orthod. 2016 Mar-Apr;21(2):45-50, where it is written:
    Ahmad Akhoundi Mohammad Sadegh, Ghazanfari Rezvaneh, EtemadMoghadam Shahroo, Alaeddini Mojgan, Khorshidian Azam, Rabbani Shahram, Shamshiri Ahmad Reza, Momeni Nafiseh.
    Should be written:
    Mohammad Sadegh Ahmad Akhoundi, Rezvaneh Ghazanfari, Shahroo Etemad-Moghadam, Mojgan Alaeddini, Azam Khorshidian, Shahram Rabbani, Ahmad Reza Shamshiri, Nafiseh Momeni.

Publication Dates

  • Publication in this collection
    Mar-Apr 2016

History

  • Received
    13 Jan 2015
  • Accepted
    17 Aug 2015
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